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The Journal of Neuroscience, December 15, 2000, 20(24):9162-9173

Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity

Holger Taschenberger and Henrique von Gersdorff

The Vollum Institute, Oregon Health Sciences University, Portland, Oregon 97201

Fast, precise, and sustained synaptic transmission at high frequency is thought to be crucial for the task of sound localization in the auditory brainstem. However, recordings from the calyx of Held synapse have revealed severe frequency-dependent synaptic depression, which tends to degrade the exact timing of postsynaptic spikes. Here we investigate the functional changes occurring throughout the critical period of synapse refinement from immature calyx terminal [postnatal day 5 (P5)] to after the onset of hearing (P12-P14). Surprisingly, for recordings near physiological temperature (35°C), we find that P14 synapses are already able to follow extremely high input rates of up to 800 Hz. This ability stems in part from a remarkable shortening of presynaptic action potentials, which may lead to a lowering of release probability and decrease in synaptic delays during development. In addition, AMPA receptor-mediated EPSCs as well as quantal synaptic currents acquired progressively faster kinetics, although their mean amplitudes did not change significantly. NMDA receptor-mediated EPSCs, however, diminished with age, as indicated by a 50% reduction in mean amplitude and faster decay kinetics. Finally, the degree of synaptic depression was greatly attenuated with age, presumably because of a 2.5-fold or larger increase in the releasable pool of vesicles, which together with a decreasing release probability produces a fairly constant EPSC amplitude. This finely tuned orchestra of developmental changes thus simultaneously promotes speed while preventing premature vesicle pool depletion during prolonged bouts of firing. A few critical days in postnatal development can thus have a large impact on synaptic function.

Key words: development; MNTB; calyx of Held; AMPA and NMDA EPSCs; quantal and mEPSCs; short-term synaptic depression; patch-clamp; neuronal reliability


Copyright © 2000 Society for Neuroscience  0270-6474/00/20249162-12$05.00/0


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C. M. Macica, C. A. A. von Hehn, L.-Y. Wang, C.-S. Ho, S. Yokoyama, R. H. Joho, and L. K. Kaczmarek
Modulation of the Kv3.1b Potassium Channel Isoform Adjusts the Fidelity of the Firing Pattern of Auditory Neurons
J. Neurosci., February 15, 2003; 23(4): 1133 - 1141.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
Y. Li and R. E. Burke
Developmental Changes in Short-Term Synaptic Depression in the Neonatal Mouse Spinal Cord
J Neurophysiol, December 1, 2002; 88(6): 3218 - 3231.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
P. D. Dodson, M. C. Barker, and I. D. Forsythe
Two Heteromeric Kv1 Potassium Channels Differentially Regulate Action Potential Firing
J. Neurosci., August 15, 2002; 22(16): 6953 - 6961.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
J. Waters and S. J Smith
Vesicle pool partitioning influences presynaptic diversity and weighting in rat hippocampal synapses
J. Physiol., June 15, 2002; 541(3): 811 - 823.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
O. Behrend, A. Brand, C. Kapfer, and B. Grothe
Auditory Response Properties in the Superior Paraolivary Nucleus of the Gerbil
J Neurophysiol, June 1, 2002; 87(6): 2915 - 2928.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
R. M. Leao and H. Von Gersdorff
Noradrenaline Increases High-Frequency Firing at the Calyx of Held Synapse During Development by Inhibiting Glutamate Release
J Neurophysiol, May 1, 2002; 87(5): 2297 - 2306.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
I. Joshi and L.-Y. Wang
Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem
J. Physiol., May 1, 2002; 540(3): 861 - 873.
[Abstract] [Full Text] [PDF]


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ScienceHome page
T. Tsujimoto, A. Jeromin, N. Saitoh, J. C. Roder, and T. Takahashi
Neuronal Calcium Sensor 1 and Activity-Dependent Facilitation of P/Q-Type Calcium Currents at Presynaptic Nerve Terminals
Science, March 22, 2002; 295(5563): 2276 - 2279.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
C. J. Meinrenken, J. G. G. Borst, and B. Sakmann
Calcium Secretion Coupling at Calyx of Held Governed by Nonuniform Channel-Vesicle Topography
J. Neurosci., March 1, 2002; 22(5): 1648 - 1667.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
S. J Pyott and C. Rosenmund
The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons
J. Physiol., March 1, 2002; 539(2): 523 - 535.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
V. Scheuss, R. Schneggenburger, and E. Neher
Separation of Presynaptic and Postsynaptic Contributions to Depression by Covariance Analysis of Successive EPSCs at the Calyx of Held Synapse
J. Neurosci., February 1, 2002; 22(3): 728 - 739.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
C.-Y. Chen, E.-h. Ling, J. M Horowitz, and A. C Bonham
Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats
J. Physiol., February 1, 2002; 538(3): 773 - 786.
[Abstract] [Full Text] [PDF]


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J. Neurophysiol.Home page
N. Chuhma and H. Ohmori
Role of Ca2+ in the Synchronization of Transmitter Release at Calyceal Synapses in the Auditory System of Rat
J Neurophysiol, January 1, 2002; 87(1): 222 - 228.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
H. Varoqui, M. K.-H. Schafer, H. Zhu, E. Weihe, and J. D. Erickson
Identification of the Differentiation-Associated Na+/PI Transporter as a Novel Vesicular Glutamate Transporter Expressed in a Distinct Set of Glutamatergic Synapses
J. Neurosci., January 1, 2002; 22(1): 142 - 155.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
S. Brenowitz and L. O. Trussell
Maturation of Synaptic Transmission at End-Bulb Synapses of the Cochlear Nucleus
J. Neurosci., December 1, 2001; 21(23): 9487 - 9498.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
A. C. Meyer, E. Neher, and R. Schneggenburger
Estimation of Quantal Size and Number of Functional Active Zones at the Calyx of Held Synapse by Nonstationary EPSC Variance Analysis
J. Neurosci., October 15, 2001; 21(20): 7889 - 7900.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
Y. Sahara and T. Takahashi
Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse
J. Physiol., October 1, 2001; 536(1): 189 - 197.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
S. Iwasaki and T. Takahashi
Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem
J. Physiol., August 1, 2001; 534(3): 861 - 871.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
K. Futai, M. Okada, K. Matsuyama, and T. Takahashi
High-Fidelity Transmission Acquired via a Developmental Decrease in NMDA Receptor Expression at an Auditory Synapse
J. Neurosci., May 15, 2001; 21(10): 3342 - 3349.
[Abstract] [Full Text] [PDF]


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J. Physiol.Home page
C.-Y. Chen, E.-h. Ling, J. M Horowitz, and A. C Bonham
Synaptic transmission in nucleus tractus solitarius is depressed by Group II and III but not Group I presynaptic metabotropic glutamate receptors in rats
J. Physiol., February 1, 2002; 538(3): 773 - 786.
[Abstract] [Full Text] [PDF]


Home page
J. Physiol.Home page
S. J Pyott and C. Rosenmund
The effects of temperature on vesicular supply and release in autaptic cultures of rat and mouse hippocampal neurons
J. Physiol., March 1, 2002; 539(2): 523 - 535.
[Abstract] [Full Text] [PDF]


Home page
J. Physiol.Home page
I. Joshi and L.-Y. Wang
Developmental profiles of glutamate receptors and synaptic transmission at a single synapse in the mouse auditory brainstem
J. Physiol., May 1, 2002; 540(3): 861 - 873.
[Abstract] [Full Text] [PDF]



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